SCIENCE ADVANCES | REVIEW ECOLOGY Copyright © 2019 The Authors, some Climate change effects on plant-soil feedbacks rights reserved; exclusive licensee and consequences for biodiversity and functioning American Association for the Advancement of terrestrial ecosystems of Science. No claim to original U.S. Government Works. Distributed Francisco I. Pugnaire1,2*, José A. Morillo1,2, Josep Peñuelas3,4, Peter B. Reich5,6, under a Creative Richard D. Bardgett7, Aurora Gaxiola2,8,9, David A. Wardle10, Wim H. van der Putten11,12 Commons Attribution NonCommercial Plant-soil feedbacks (PSFs) are interactions among plants, soil organisms, and abiotic soil conditions that influence License 4.0 (CC BY-NC). plant performance, plant species diversity, and community structure, ultimately driving ecosystem processes. We review how climate change will alter PSFs and their potential consequences for ecosystem functioning. Climate change influences PSFs through the performance of interacting species and altered community composition resulting from changes in species distributions. Climate change thus affects plant inputs into the soil subsystem via litter and rhizodeposits and alters the composition of the living plant roots with which mutualistic symbionts, decomposers, and their natural enemies interact. Many of these plant-soil interactions are species-specific and are greatly affected by temperature, moisture, and other climate-related factors. We make a number of predictions concerning climate change effects on PSFs and consequences for vegetation-soil-climate feedbacks while acknowledging that they may be context-dependent, spatially heterogeneous, and temporally variable. INTRODUCTION the microbial processes that underlie changes in PSFs, such as climate Plants and soils are inextricably linked. Plants alter soil properties, change–induced alterations in the balance of pathogenic and mutualistic which, in turn, influence plant performance, displaying a variety of taxa or saprophytic microbial taxa that mediate plant nutrient supply, effects on each other. These effects of plants on themselves, their is challenging and requires identifying the individual contribution offspring, and other plant species through influences on soil organisms of the various soil biotic components to PSFs (8). and abiotic soil conditions are termed plant-soil feedbacks (PSFs) (1–5). Here, we address the responses of PSFs to climate change and their The interaction between plants and their associated soil biota can lead consequences for biodiversity, ecosystem functioning, and potential to complex feedbacks that regulate plant community dynamics and feedback effects to climate change. We first consider how soil microbes ecosystem processes. The net outcome of PSFs on plant growth depends control PSFs, because the vast diversity of beneficial and pathogenic on the balance between antagonistic and beneficial interactions with microorganisms that interact with plant roots or feed on detritus and the extant plant and soil microbial communities, which can vary rhizodeposits can directly affect plant performance (9, 10). We then focus depending on both biotic (e.g., plant functional traits) and abiotic on how climate change may alter primary and secondary succession by (e.g., soil pH, physical structure, and nutrient availability) factors (6). affecting PSFs, which are often important drivers of plant species re- Climate is one of the main drivers of organism growth and species placement. Soil communities contain a myriad of species that comprise distributions; thus, a changing climate has the potential to alter the a trophic network of primary producers and consumers, and of composition of plant and soil communities and the interactions between secondary and higher-level consumers (11) that could be altered by them. However, very little is known about the underlying mechanisms changing climate (12). We thus focus on how climate change affects PSFs involved and the consequences for feedbacks to climate. In particular, and soil food webs, with emphasis on both the impacts of increased most studies of PSFs have examined the role of soil microbial temperature and climate extremes, especially drought (12). We then communities, focusing on net effects of all microbes involved in outline how climate change will affect litterfall and the production influencing plant performance positively and negatively (7). Identifying of root exudates, which control the structure and dynamics of soil communities. Last, we focus on how increased levels of atmospheric 1 CO2 directly (i.e., not indirectly via a changing climate) influence PSFs, Estación Experimental de Zonas Áridas, Consejo Superior de Investigaciones Científicas, Carretera de Sacramento s/n, La Cañada de San Urbano, E-04120 Almería, which will occur simultaneously with its feedback effects to climate. Spain. 2Laboratorio Internacional en Cambio Global (LINCGlobal). 3Consejo Superior By discussing PSFs and climate in combination, and the con- de Investigaciones Científicas, Global Ecology Unit CREAF-CSIC-UAB, Bellaterra, sequences for feedbacks from vegetation-soil to climate, our over- Catalonia E-08193, Spain. 4CREAF, Cerdanyola del Vallès, Catalonia E-08193, Spain. riding goals are to anticipate how climate change may affect plant 5 Department of Forest Resources, University of Minnesota, St. Paul, MN 55108, USA. 6 Hawkesbury Institute for the Environment, Western Sydney University, Penrith, and soil communities, to derive some generalizations about how NSW 2753, Australia. 7Department of Earth and Environmental Sciences, The a changing climate may affect PSFs and consequences for key University of Manchester, Michael Smith Building, Oxford Road, Manchester M13 community and ecosystem-level properties and climate, as well as 9PT, UK. 8Departamento de Ecología, Pontificia Universidad Católica de Chile, Alameda 340, Santiago, Chile. 9Instituto de Ecología y Biodiversidad, Las Palmeras to identify important knowledge gaps. 3425, Santiago, Chile. 10Asian School of the Environment, Nanyang Technological University, 50 Nanyang Avenue, 639798, Singapore. 11Department of Terrestrial Ecology, Netherlands Institute of Ecology, Post Office Box 50, 6700 AB Wageningen, MICROBIAL CONTROLS ON PSFs Netherlands. 12Department of Nematology, Wageningen University, 6708 PB Wageningen, Netherlands. Soil microorganisms can affect PSFs in complex ways. For example, *Corresponding author. Email: fip@eeza.csic.es the accumulation of host-specific pathogenic fungi in the rhizosphere Pugnaire et al., Sci. Adv. 2019; 5 : eaaz1834 27 November 2019 1 of 11 SCIENCE ADVANCES | REVIEW is an important driver of negative PSFs, with consequences for plant that could help enhance our capacity to predict PSFs and vegetation species coexistence and diversity-productivity relationships (13–15). dynamics in terrestrial ecosystems (Table 1). For instance, some Conversely, positive PSFs are typically associated with the accumulation studies show a consistent role of mycorrhizal type in influencing PSFs of not only beneficial microorganisms in the rhizosphere, especially at multiple scales (24) and reveal the importance of plant traits, mycorrhizal fungi (16–17), but also nitrogen (N)–fixing symbionts especially those related to nutrient acquisition strategy, for explaining (18–19). PSFs can also become more positive or less negative because PSFs (19, 28). Furthermore, while it is unknown as to how interactions of free-living soil bacteria and fungi involved in the decomposition of between plants and soil biotic communities will evolve in response to organic matter (20) and the transformation of plant growth–limiting proxies of climate change, it is likely that they will affect the outcome nutrients (21). of PSFs with potential consequences for vegetation dynamics, ecosystem Recent evidence suggests that PSFs involve myriad interactions processes, and feedback effects to climate. For example, drought can among a diversity of beneficial and antagonistic microbes. For example, alter soil bacterial and fungal communities and modify the direction of the same graminoid microbial [arbuscular mycorrhizal (AM) fungi] PSFs and plant competitive interactions (21); soil bacterial communities partners can shift from beneficial to antagonistic depending on in the tropics and at high latitudes are subjected to stronger environmental microsite conditions (22). Similarly, although AM fungi are often filtering and include more edaphic-niche specialists, possibly rendering beneficial to trees (23), tree species with AM fungi have also been these communities more vulnerable to global change (35). As such, shown to more often experience negative feedback in comparison climate change is likely to have both strong direct effects on plants to ectomycorrhizal (EM) trees, which predominantly display positive and soil organisms, as well as indirect effects through changes in feedback (24, 25). In addition, studies reveal that these effects of plant physiology and the quality and quantity of resources entering soil fungi on PSFs vary across fungal guilds (26): Feedbacks might soil (i.e., as litter and rhizodeposits) (Fig. 2). This will, in turn, have become more negative as the richness of plant pathogens and potentially large consequences for PSFs, vegetation dynamics, and specialist decomposers increases and become more positive as the feedback effects to local or even global climate conditions. In sum, diversity of AM fungi increases (25, 26). These studies show that PSFs and despite the complexity and high variety of processes involved, may depend on plant interactions with highly diverse rhizospheric our ability to make predictions involving PSFs is improving, and in the microbial communities rather than with single host-specific pathogens future, it should increasingly be possible to apply this knowledge to or mutualistic symbionts (14, 25, 26). address environmental challenges such as climate change mitigation Climate change can modify the direction and intensity of microbial-­ or ecosystem restoration by using nature-based solutions, as well as mediated PSFs through a variety of mechanisms. For example, the informing conservation policies. alteration of soil microbial communities by climatic extremes, such as recurring droughts, can modify both the direction and intensity of PSFs, with consequences for plant-plant interactions and invasiveness TEMPERATURE AND DROUGHT EFFECTS ON (21, 27–28). The adaptation of soil microbial communities to drought PLANT-SOIL INTERACTIONS can also improve plant fitness (29) and favor mycorrhizal fungi and Climate change alters plant-derived inputs to soil in the form of litter symbiotic soil bacteria, which enhance the tolerance of plants to production and rhizodeposition, raising questions about the way and drought (30) and presumably influence PSFs. Warming and altered intensity with which they are affected (37, 38). If terrestrial plant precipitation will also modify PSFs, hence plant-plant interactions, productivity does increase with warming by increasing nutrients by altering belowground pathogen pressure and root associations available from decomposition, then more litterfall may be expected. with mutualistic symbionts and/or by decoupling range-expanding However, higher temperatures affect plant physiology and lead to plants from their host-specific soil communities, including pathogens higher evaporation and plant transpiration, exacerbating water shortage (Fig. 1) (31). Changes in plant physiology and phenology caused by effects. In addition, acclimation to warming is likely to dampen climate change, although poorly understood, can alter soil microbial potential responses. Climate change is also expected to increase the communities via changes in rhizodeposition (i.e., the release of intensity and frequency of climate extremes, for instance, through resources from plant roots into the soil), thereby potentially modifying increased drought periods and periodically extreme rainfall conditions. the microbial-mediated PSFs (32, 33) and the capacity to change Some studies simulating moderate drought conditions in extratropical feedback effects from soil and vegetation to climate. ecosystems counterintuitively found an increase in aboveground litter Evidence suggests that climate change may affect the biodiversity production, but only in the short term (39). By contrast, studies from and function of soil microbes. Rainfall timing plays a critical role on the humid and subhumid tropical forests found no changes or only slight abundance and diversity of soil microbial populations in grasslands decreases in the production of aboveground litter under moderately (34), and the diversity of microbial gene functions in topsoil microbial induced drought (40). Persistent drought, however, leads to species communities is strongly correlated with precipitation, suggesting turnover and less aboveground biomass, resulting in less litter production a clear association between specific microbial metabolic functions (39, 40). Increasing aridity in geographical gradients also results in and climate (35). Drought legacy effects influence the composition of decreased aboveground litter production (41). The quality of litter soil fungal and bacterial communities via specific response groups decreases with drought in all biomes, even if total litterfall remains composed of members with broad phylogenetic origins, including constant, partly because of elevated nutrient resorption prior to leaf rare taxa (36). This suggests that rare taxa should not be overlooked senescence (42) and the production of carbon-based, recalcitrant when modeling microbial responses to climate change and their structural compounds under drought (Fig. 2). These changes not only potential consequences for plants. slow down mineralization rates, nutrient release, and nutrient cycles Key microbial processes involved in potential change of PSFs are that may increase or decrease plant diversity through species turnover, context dependent and differ across ecosystems and with the plant depending on environmental conditions (43, 44), but also affect CO2 species involved. However, some generalities are beginning to emerge release to the atmosphere and therefore feedback to climate. Pugnaire et al., Sci. Adv. 2019; 5 : eaaz1834 27 November 2019 2 of 11 SCIENCE ADVANCES | REVIEW A B Fig. 1. Alteration of trophic relationships depending on responses to climate change. Arrows indicate CO2 flow; solid arrows represent net input, and dashed arrows represent net output, with arrow thickness proportional to flow. Circles show different species in a simplified soil food web. The unperturbed system prior to the onset of a chronic global change driver (A) gives way to a long-term response (B) in which poorly performing plant species and their pathogens or symbionts are lost from the system, and new, more competitive plant species that have escaped their natural enemies are added to the community. As a result, the biomass of nonspecialist mutualists or pathogens increases, and the biomass of one decomposer group remains high [modified from (37)]. Table 1. Summary of expert assessment of potential impacts of climate change drivers (positive, negative, or neutral) on PSFs based on the general effects of known environmental conditions on soil communities. Climate change drivers PSF type Warming Drier conditions Wetter conditions Fire Increased CO2 Fungi Pathogens +++ −− +++ −− 0 Saprotrophic/organic ++ −− +++ −− ? matter decomposers AM fungi +++ +++ + −−− ? EM fungi + −−− + −−− + Bacteria Pathogens +++ −− +++ −− ? Symbiotic N fixers 0 −−− ++ 0 + Nonsymbiotic N fixers 0 −− ++ 0 + Drought-tolerant + +++ −− 0 ? microbes Other specific coevolved +++ −−− ++ ++ ? microbes Other Primary detritivorous ++ −− ++ −− ? invertebrates Secondary detritivorous ++ −− ++ − ? invertebrates Root herbivores ++ −− ++ 0 ? Pugnaire et al., Sci. Adv. 2019; 5 : eaaz1834 27 November 2019 3 of 11 SCIENCE ADVANCES | REVIEW Plant community Fast-growing species Slow-growing species Humid Drought High High- Low- Low nutrient quality quality nutrient availability litter litter availability Bacteria Fungi Fig. 2. Effects of drought on litter productivity and species turnover and their relationships with PSFs. Drought leads to low-quality litter with recalcitrant carbon (C) compounds and low nutrient content. This litter is difficult to decompose and determines a fungal-dominated microbial community composition while decreasing the availability of nutrients for plants. These conditions lead to a replacement by plant species that are better adapted to drought conditions, in contrast to more humid conditions where nutrient-rich litter is fast decomposed by bacterial-dominated microbial communities. Arrows indicate carbon flow; solid arrows represent net input, and dashed arrows represent net output, with arrow thickness proportional to flow. Increasing aridity can cause large changes in nutrient cycling and PSFs AND FOOD WEB DYNAMICS enhances the impact of ultraviolet radiation on litter decomposition Microbes are part of a complex soil food web, which consists of (45, 46), which may cause an imbalance in nutrient cycling with numerous species or taxa across different trophic levels, including negative effects on plant diversity (47). Decreases in plant growth primary producers (plant roots and algae), primary consumers and belowground carbon allocation in grasslands as a consequence (bacteria, archaea, fungi, viruses, and root-feeding fauna), and of drought have also been reported (48), and drought has legacy secondary and higher-level consumers (bacterivores, fungivores, and effects on soil microbial communities that can affect plant-plant predators) (10, 50). These organisms are all important components interactions (21) and even neutralize PSFs through increased water of the plant-soil system that are able to alter the outcome of PSFs demand linked to higher nutrient demand with positive PSFs (28). (51). Although widely acknowledged as important drivers of soil In dry ecosystems, soil microbes can buffer the negative effects of biogeochemical processes modulated by climate (52), soil food webs drought on seed germination and plant growth in a species-specific show high interactivity and complexity (11). Climate change effects way, so that plants such as legumes that are more dependent on on soil food webs will be affected by the fact that combined responses specific coevolved microbes are more sensitive and less buffered by of the individual components of PSFs—decomposers, mutualistic soil microbiota than other species (49). PSFs also play a key role in symbionts, and herbivores/pathogens—are all influenced (Fig. 3) (7). plant recruitment by influencing seed germination and seedling However, the net effects will be difficult to predict when we consider establishment, which are, in turn, important in regulating plant all the individual components of the soil biota in isolation. The diversity and community dynamics (14). The susceptibility of different elegance of the PSF concept is that the overall functional consequences plant species to soil biota determines their relative abundance, as of climate change on the soil biota can be assessed through its combined soil pathogens reduce recruitment and survival of different species impact on plant performance and, ultimately, the net PSF effect. This (2). In contrast, other soil microorganisms offer protection from may also have implications for extremely long-term patterns in PSFs. pathogens or modify nutrient availability, thereby benefitting some For example, body size of soil invertebrates decreased during the dry plant species over others (7). Our knowledge on how PSFs can affect and warm conditions in the Paleocene-Eocene Thermal Maximum, plant communities and ecosystem dynamics can help us forecast affecting ecosystem functions such as organic matter decomposition potential trajectories of ecosystem change under different climate and nutrient cycling, which, in turn, affected plant diversity (53). change scenarios. The consequences of these long-term effects on the soil food web Pugnaire et al., Sci. Adv. 2019; 5 : eaaz1834 27 November 2019 4 of 11 SCIENCE ADVANCES | REVIEW AG plant consumers Temperature Moisture Litter BG plant decomposition consumers BG mutualists BG top-down control Fig. 3. Depiction of effects of abiotic and biotic drivers on PSFs. Drivers such as temperature (1), moisture (2), aboveground (AG) plant consumers (3), and below- ground (BG) top-down control (4) impact on several components of PSFs (e.g., BG mutualists, plant consumers, and litter decomposition) are shown. Orange ovals show the abiotic and biotic drivers of PSF components, shown in dashed circles. PSF components control whether the feedback response is positive or negative. Temperature, moisture, and aboveground plant consumers can also directly affect plant performance (5 to 7). Abiotic and biotic drivers could interact with each other (circle connecting the drivers), and this will affect the way that each one affects the components of PSFs [based on (108)]. for PSFs have not yet been assessed. The influence of climate change released from negative PSFs (58). In the new range, PSFs are expected may also affect plant community composition through mechanisms to become more negative over time because of pathogen accumulation such as shrub encroachment, as discussed in the section on succession. (59); in the meantime, range-shifting plant populations may have If water and nutrients become limiting, the role of mutualistic invasive characteristics and potentially reduce local native plant symbionts in the soil food web, which are involved in plant nutrient biodiversity (60). Range shifts seem to have much weaker effects on acquisition and drought tolerance, may increase: AM fungi and plant-mutualist symbiotic relationships and plant-decomposer N fixers both lead to positive PSFs, which can promote primary interactions than on other plant-microbe interactions, possibly due production if all other conditions remain unaltered (54). This scenario to the lower degree of host specificity of these microbes. Thus, may also affect plant community composition, with an increased direct effects of climate on temperature and rainfall, along with dominance of plant species that fix N and/or those forming AM species range shifts, are likely to affect PSFs. PSFs during range (55). These plant species, however, are not necessarily less influenced shifts under climate change will most likely turn from negative in by soil-borne pathogens (24), and PSFs may easily become more the home range to less negative, or even positive in the new range. negative, because climatic extremes may increase the vulnerability However, these effects can be dynamic when considering longer time of plants to herbivores or pathogens (56). periods and are ultimately expected to become more negative over time because of cointroduction of the native pathogens or evolutionary developments of local pathogens (60). PSFs AND RANGE EXPANSION The type and timing of climatic extremes may be crucial for the An important element of climate change is range shifts of plants, dynamics and range expansion of plant communities. Drought or soil animals, and microbial taxa over time (12, 35). Range-shifting extreme rainfall may occur before or during the growing season, plant species have fewer negative PSF effects in their new range (57). and their effects on plant community composition can differ. In a Few studies have compared PSF effects between the original and new greenhouse study (27), plant species that expanded their range from ranges but suggest that range shifts enable plant species to become southern Europe (warm and dry) toward northern Europe (currently Pugnaire et al., Sci. Adv. 2019; 5 : eaaz1834 27 November 2019 5 of 11 SCIENCE ADVANCES | REVIEW warming) were grown in mixed communities with their congeneric taining high soil nutrient availability where fast-growing species relatives that were native to northern Europe. The soils in that study thrive (Fig. 2). had been subjected to preseason drought, preseason rainfall, and In addition to leaf litter, rhizodeposition is a large source of combined conditions and were then brought back to control soil organic matter entering the soil that will be affected by climate water conditions. Preseason drought increased the proportional change. Rhizodeposits are highly dependent on plant physiological contribution of range-expanding plant species to community activity, which will be affected by expected changes in climate. composition, whereas preseason rainfall had smaller effects (27). These Changes in exudate composition, not just quantity, may also have effects corresponded to the increased abundance of the so-called crucial impacts on soil properties and organisms. Under drought, “drought response types” or “wet response types” among both plants exudate more secondary compounds (including antioxidants), bacteria and fungi (36). Furthermore, a recent outdoor mesocosm phytohormones, soluble sugars and compounds that act as osmolytes study (61) compared the current climatic situation with three future (73, 74), as well as metabolites such as proline (75) that buffer the scenarios: range shifts of plants but not soil biota, range shifts of soil cellular redox status during drought. Drought-driven changes in biota but not plants, and range shifts of both plants and soil biota. rhizodeposition, thus, have complex effects on bacterial and fungal During the growing season, half of the mesocosms were exposed to communities. The changes depend on the intensity of the drought drought, while the other half was provided with the 30-year average and previous soil history. Bacteria may be more negatively affected water conditions of nondrought years. During extreme drought, than fungi in terms of biomass stock. The resulting shift toward a decomposition was strongly reduced in all four types of mesocosms. relative increase in fungi and a relative decrease in the biomass and After rewetting the soil, however, decomposition with plants in diversity of bacteria (76) is likely to affect food webs and plants temperate zones recovered 2 weeks faster than that with range-shifted by generating different availabilities of nutrients (43). In addition, plants that originated from a region characterized by severe summer altered microbial communities would feed back to the extant plant droughts. community through altering organic matter decomposition (77, 78) Recent evidence suggests that range shift of plant species as a and nutrient uptake (79), likely leading to different patterns of species consequence of climate change may be essential for the adaptation replacement. Thus, climate change impacts on plant-soil interactions of ecosystems to novel climatic conditions (62). However, when will have consequences for the carbon cycle, and a potential decoupling range-expanding plant species have invasive properties, they may of plant-soil interactions may happen as if plants undergo a range change ecosystem processes, for example, through altered nutrient shift while their associated soil communities do not. This decoupling cycling and interactions with above- and belowground biota (63). is a largely unrecognized, but potentially important, regulator of the Moreover, range expanders may also respond differently to extreme future global carbon cycle (37). weather events than will native plant species. Managing these types of changes in ecosystems will be crucial, and the maintenance of soil biodiversity is expected to ensure soil functioning under a variety of HOW CLIMATE AFFECTS PSF CONTROL OF SUCCESSION novel climatic conditions (50). PSFs are often important drivers of plant species replacement and, thus, succession, which includes impacts of both soil biota associated with plant roots and those involved in the decomposer subsystem LITTER TRAITS AND DECOMPOSITION UNDER CLIMATE CHANGE (80). Given that disturbance associated with climate change may Climatic factors, such as temperature and rainfall, are critical controls increase in the future (e.g., more fires, more windthrow), impacts of litter decomposition, and these factors interact with local plant and on, and consequences of, PSF-driven succession will likely increase soil communities (64, 65). Relationships based on climatic averages in importance. Feedbacks between early successional plant species conceal much of the local variability, and the response of this local and their root-associated soil biota frequently contribute to the variability to climate change will determine how climate change is replacement of these species by other species. This replacement may likely to influence global patterns of litter decomposition (66). arise, for example, by early successional species promoting the The turnover of plant species due to climate change can greatly accumulation of soil pathogens that negatively affect them (4, 81) affect litter decomposition (Fig. 2) (67). Field and laboratory experiments or by forming mutualisms with symbiotic N-fixing bacteria that have shown that litter quality determines the functional characteristics improve soil fertility and thereby facilitate later successional species of the soil decomposer community. Recalcitrant litter can contain that outcompete them (82). By contrast, late successional species considerable amounts of polyphenols (e.g., phenolic acids and often form positive associations with their soil biota and, notably, flavonoids) or polymers (e.g., condensed tannins) that require high with mycorrhizal fungi, which slows succession. For example, along activation energy (68) and inhibit microbial decomposition (69). a chronosequence of Dutch (old field) grasslands on abandoned Recalcitrant litter would, however, promote microbial communities arable land, early successional plant species consistently underwent specialized in degrading complex plant polymers (70), so slow negative feedbacks with their soil biota, while late successional plants microbial metabolism and nutrient release will favor slow-growing only underwent positive feedbacks (83). PSFs involving soil biota can plant species. Furthermore, under warmer and drier conditions, also alter plant succession by altering the supply of soil nutrients fungal metabolism can shift toward maintenance at the expense of the available to plants. Decomposer biota can thus accelerate succession by production of enzymes that break down plant-carbon compounds, mineralizing nutrients that facilitate later successional species that with concomitant effects on plant communities and ecosystem then outcompete earlier species (84), or succession can be retarded if carbon dynamics (71). Under different scenarios, it is likely that plants produce recalcitrant litter that can be better metabolized by communities dominated by fast-growing species will continue to their own mycorrhizal symbionts than by those of other species (85, 86). produce high-quality litter, which may promote soil microbial Although we have some understanding of how PSFs influence communities that will decompose litter at faster rates (72), main- plant succession, we have limited knowledge on how these effects Pugnaire et al., Sci. Adv. 2019; 5 : eaaz1834 27 November 2019 6 of 11 SCIENCE ADVANCES | REVIEW are mediated by climate or how they might be altered by ongoing or has neutral or negative effects on decomposition and nutrient climate change. Explicitly addressing this issue will require studies cycling. The former PSFs allow the responses of plant biomass to eCO2 that directly consider the interactive effects of macroclimatic variables to remain stable or grow stronger (the “priming” effect), whereas and succession; few studies have used such an approach (87–89), the latter PSFs contribute to, and perhaps increase, the extent of the and none of them have explicitly studied PSFs. However, the work constraints of nutrient limitation on the use of eCO2 by plants. This by Laliberté et al. (89) does offer some insights. Here, plant biomass is a major puzzle in eCO2 science because many kinds of effects, for and the structure of the soil food web were investigated across each instance, increased, neutral, or decreased soil nutrient cycling in of the four parallel chronosequences formed on the same parent response to eCO2, have been reported (96–98). This puzzle is also a material in Western Australia; these four sequences differ in both key issue for society, and the questions of whether or how much the temperature and moisture balance within the range of what would be direct effects of eCO2 stimulate a negative feedback from terrestrial expected for future climate change. They showed that chronosequence ecosystems that reduces the rate of global warming [by additional stage was the most important driver of the soil food web, with little carbon (C) sequestration] are poorly understood. This sequestration interactive effect of stage with climate. Given that the soil food web requires an increase in C uptake by plants and a neutral, negative, or governs nutrient supply rates from the soil, which then affects positive return of C to soil (by autotrophic and heterotrophic respiration) successional processes, this study suggests that variation in the that is smaller than the uptake. Soil microbes play a key role both ecological impact of the soil food web and, ultimately, its impacts of because they control the supply of nutrients to plants and thus the PSFs among (versus within) successional gradients of contrasting magnitude of increase in the response of biomass to eCO2 and climate is probably not large. This study does not, of course, directly because they determine the rate of decomposition of both new and address the question about how climate determines the role of PSFs in old C in soils. driving succession, and it remains unknown whether the results of Organisms at higher trophic levels play a role in the soil food this study are likely to apply to successional gradients elsewhere, but it web, but two groups of soil microbes have particularly important offers insights into how this question could be explicitly addressed. roles in these processes and, thus, in the responses of terrestrial At a broad level of resolution, the types of above- and belowground ecosystems to eCO2: the mutualistic mycorrhizal fungi and heterotrophic biotic changes that occur during succession and ecosystem development decomposers (99). Their characteristics and tendencies may help appear to be relatively constant among regions that experience very us solve the puzzle of the eCO2 responses outlined above. They different climatic regimes (89–91). Therefore, the biggest effects of are important because (i) nutrient limitation on plant responses to climate change in driving how soil biota and PSFs affect succession eCO2 may be modulated by the type of nutrient-acquisition strategy, are likely to be driven by finer-scale factors such as what types of which, in turn, may be largely determined by mutualistic symbiotic plants in any given environment will or will not be favored by future plant-microbe interaction, and (ii) eCO2 may increase nutrient climate. For example, shrub encroachment of subarctic tundra cycling or have neutral or suppressive effects due to the regulation by resulting from climate change (92) involves successional pathways and impacts on both mycorrhizae and decomposer communities. moving toward domination by woody plants that show positive Plant species associated with EM fungi have a stronger response feedbacks with ericoid and EM fungi. Conversely, in some temperate of biomass to elevated eCO2 when soil has more available N, whereas regions, warming should lead to successional pathways involving plant species associated with AM fungi increase biomass more under domination by trees that undergo feedbacks with AM fungi rather eCO2 when soils have more available P (100). These responses are than with EM and saprophytic fungi (93). Increasing aridity in tropical partly due to the lower cost and thus higher return on investment regions may promote early successional species that form positive for acquiring additional N under eCO2 when associating with EM associations with N-fixing bacteria (94, 95), thereby eventually rather than AM fungi (100). EM plants, however, decrease soil C benefitting later successional species. There are numerous examples pools via priming (i.e., the stimulation or suppression of soil organic of where specific plant functional types are likely to enter or exit matter decomposition by live roots and associated rhizosphere successional pathways due to climate change, and while each of these organisms) (99), offsetting the scope of their potential increased C will have their own feedbacks with their associated soil biota, the sequestration induced by eCO2. nature and direction of these feedbacks are likely to be case specific. Long-term eCO2 also influences soil decomposer communities Understanding the mechanisms underlying this context dependency in ways that likely influence decomposition and the potential storage is key to understanding and predicting how successional pathways of soil C. For example, eCO2 in a long-term eCO2 experiment in develop under a changing global climate and, therefore, the dominant perennial grassland led to distinct microbial communities (101). types of vegetation that are likely to result. The abundances of key C-fixation genes; some C-degrading genes involved in the decomposition of starch, cellulose, and hemicellulose; and functional genes involved in N cycling were also higher (102, 103). PSF RESPONSES TO ELEVATED CO2 These changes in soil microbial communities and their functional We have so far referred mostly to climate, but the direct effects of genes and enzymatic production likely play key roles in the faster elevated CO2 (eCO2) may be important as well. In addition, any decomposition of soil organic matter under eCO2. effect of climate change on PSFs will happen within the context of Our understanding of whether or how eCO2 will drive complex rising CO2 effects on PSFs; hence, consideration of both direct CO2 interactions of soil communities in space and time remains limited, and direct and indirect effects of climate change seems essential to despite the considerable advances briefly outlined above. For example, develop a holistic, integrated perspective. A critical question involving a 20-year free-air CO2 enrichment study found that the impact of the impacts of eCO2 on PSFs is whether eCO2 stimulates the soil eCO2 on microbial-mediated nutrient cycling and, consequently, community to increase the rates of decomposition and associated on the responses of biomass to eCO2 can change over time in ways N and phosphorus (P) cycling through increased plant productivity, unpredicted by theory because of poorly understood mechanisms Pugnaire et al., Sci. Adv. 2019; 5 : eaaz1834 27 November 2019 7 of 11 SCIENCE ADVANCES | REVIEW (103). The impacts of eCO2 on soil N cycling in this study shifted 1. As the types of above- and belowground biotic changes that from positive to negative over time in C3 grass communities and occur during succession are relatively constant across regions with from negative to positive over time in C4 grass communities. These very different climates, we predict that the role of PSF in succession shifts in N cycling contributed to parallel shifts in the responses of might not be greatly altered by climate change. biomass to eCO2; biomass enhancement due to eCO2 disappeared 2. However, how plant functional types exiting or entering suc- over time in the C3 grass communities and increased over time in cessional pathways respond to climate change and the role of PSFs the C4 grass communities. Changes in the composition, abundance, in mediating this response are likely to be case specific. and function of both mycorrhizal and decomposer communities 3. Enhancing the sustainability of ecosystem function both likely played influential roles in these temporal shifts, but we have above- and belowground may require promotion of the fungal neither the empirical evidence to characterize that pattern nor a component in soils because soils dominated by fungi are more sufficient theoretical foundation to conceptually explain it convincingly. stable under extreme droughts and more able to retain nutrients, The possibility that long-term changes in soil communities, including which thus limits nutrient losses from soil. their responses to eCO2 and cascading biogeochemical impacts, may 4. Climate change–induced shifts in plant distribution may en- follow a diversity of possible pathways that are broader than we have able plants to become released from negative PSF for a prolonged anticipated suggests that we should be cautious in our confidence to period (decades or longer). In their new range, some range-shifting predict these interactions, or their consequences, in the long term. plant species therefore may show invasive dominance. This caution becomes even more apparent when we consider the 5. Extreme weather events resulting from climate change may also potential interactions among eCO2, temperature, and/or moisture alter PSFs in such a way as to promote the dominance of introduced on soil communities and PSFs (104, 105). exotic species. 6. Invasive species outbreaks fostered by climate change may be controlled by negative PSFs in biodiversity-rich ecosystems. UNSOLVED QUESTIONS 7. 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